(Cryptic) sex in the microsporidian Nosema granulosis - Evidence from parasite rDNA and host mitochondrial DNA

Infection, Genetics and Evolution

Volumn 21, Issue , 2014, Pages 259-268

  Krebes, Lukas ^a   Zeidler, Lisza ^a   Frankowski, Jens ^a   Bastrop, Ralf ^a  

^a UNIVERSITY OF ROSTOCK   (Germany)

Author keywords

Microsporidia; Mode of transmission; Nosema; RDNA; Recombination; Sexual reproduction

Indexed keywords

MITOCHONDRIAL DNA; RIBOSOME DNA; SMALL SUBUNIT RIBOSOMAL RNA; SPACER DNA; FUNGAL DNA;

ARTICLE; ASEXUAL REPRODUCTION; COX1 GENE; DNA RECOMBINATION; DNA SEQUENCE; GAMMARUS DUEBENI; GENE; GENETIC VARIABILITY; HAPLOTYPE; HOST PARASITE INTERACTION; INHERITANCE; MICROSPORIDIA; MOLECULAR EVOLUTION; NONHUMAN; NOSEMA GRANULOSIS; PHYLOGENY; PRIORITY JOURNAL; SEXUALITY; AMPHIPODA; ANIMAL; CLASSIFICATION; FUNGAL MATING TYPE GENE; GENETIC RECOMBINATION; GENETICS; MICROBIOLOGY; MOLECULAR GENETICS; NOSEMA; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; STATISTICAL MODEL;

ANIMALIA; CRUSTACEA; EUKARYOTA; GAMMARUS DUEBENI; MICROSPORIDIA; NOSEMA; NOSEMA GRANULOSIS; VAIRIMORPHA;

AMPHIPODA; ANIMALS; BASE SEQUENCE; DNA, FUNGAL; DNA, MITOCHONDRIAL; DNA, RIBOSOMAL; GENES, MATING TYPE, FUNGAL; GENETIC VARIATION; MODELS, STATISTICAL; MOLECULAR SEQUENCE DATA; NOSEMA; PHYLOGENY; RECOMBINATION, GENETIC;

EID: 84890073800     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2013.11.007     Document Type: Article

References (91)

1. Avise J.C., Shapira J.F., Daniel S.W., Aquadro C.F., Lansman R.A. Mitochondrial DNA differentiation during the speciation process in Peromyscus. Mol. Biol. Evol. 1983, 1:38-56.
2. Bandelt H.J., Forster P., Röhl A. Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 1999, 16:37-48.
3. Birky C.W. Heterozygosity, heteromorphy, and phylogenetic trees in asexual eukaryotes. Genetics 1996, 144:427-437.
4. Boni M.F., Posada D., Feldman M.W. An exact nonparametric method for inferring mosaic structure in sequence triplets. Genetics 2007, 176:1035-1047.
5. Bruen T.C., Philippe H., Bryant D. A simple and robust statistical test for detecting the presence of recombination. Genetics 2006, 172:2665-2681.
6. Cristescu M.E.A., Hebert P.D.N. Phylogeny and adaptive radiation in the Onychopoda (Crustacea, Cladocera): evidence from multiple gene sequences. J. Evol. Biol. 2002, 15:838-849.
7. Cristescu M.E.A., Hebert P.D.N., Onciu T.M. Phylogeography of Ponto-Caspian crustaceans: a benthic-planktonic comparison. Mol. Ecol. 2003, 12:985-996.
8. de Sousa Queiroz C., Batista F.R., de Oliveira L.O. Evolution of the 5.8S nrDNA gene and internal transcribed spacers in Carapichea ipecacuanha (Rubiaceae) within a phylogeographic context. Mol. Phylogenet. Evol. 2011, 59:293-302.
9. Denduangboripant J., Cronk Q.C. High intraindividual variation in internal transcibed spacer sequences in Aeschynanthus (Gesneriaceae): implications for phylogenetics. Proc. Biol. Sci. 2000, 267:1407-1415.
10. Do C.B., Mahabhashyam M.S., Brudno M., Batzoglou S. ProbCons: probabilistic consistency-based multiple sequence alignment. Genome Res. 2005, 15:330-340.
11. Dunn A.M., Rigaud T. Horizontal transfer of parasitic sex ratio distorters between crustacean hosts. Parasitology 1998, 117:15-19.
12. Dunn A.M., Smith J.E. Microsporidian life cycles and diversity: the relationship between virulence and transmission. Microbes Infect. 2001, 3:381-388.
13. Dunn A.M., Hatcher M.J., Terry R.S., Tofts C. Evolutionary ecology of vertically transmitted parasites: transovarial transmission of a microsporidian sex ratio distorter in Gammarus duebeni. Parasitology 1995, 111:91-109.
14. Dunn A.M., Terry R.S., Taneyhill D.E. Within-host transmission strategies of transovarial, feminizing parasites of Gammarus duebeni. Parasitology 1998, 117:21-30.
15. Dunn A.M., Andrews T., Ingrey H., Riley J., Wedell N. Strategic sperm allocation under parasitic sex-ratio distortion. Biol. Lett. 2006, 2:78-80.
16. Edgar R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32:1792-1797.
17. Edgar R.C. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 2004, 5:113. 10.1186/1471-2105-5-113.
18. Eickbush T.H., Eickbush D.G. Finely orchestrated movements: evolution of the ribosomal RNA genes. Genetics 2007, 175:477-485.
19. Erickson B.W., Blanquet R.S. The occurrence of chitin in the spore wall of Glugea weissenbergi. J. Invertebr. Pathol. 1969, 14:358-364.
20. Excoffier L., Smouse P., Quattro J. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 1992, 131:479-491.
21. Excoffier L., Laval G., Schneider S. Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol. Bioinform. Online 2005, 1:47-50.
22. Gatehouse H.G., Malone L.A. The ribosomal RNA gene region of Nosema apis (Microspora): DNA sequence for small and large subunit rRNA genes and evidence of a large tandem repeat unit size. J. Invertebr. Pathol. 1998, 71:97-105.
23. Gibbs M.J., Armstrong J.S., Gibbs A.J. Sister-scanning: a Monte Carlo procedure for assessing signals in recombinant sequences. Bioinformatics 2000, 16:573-582.
24. Goldman A.S.H., Lichten M. The efficiency of meiotic recombination between dispersed sequences in Saccharomyces cerevisiae depends upon their chromosomal location. Genetics 1996, 144:43-55.
25. Haag K.L., Traunecker E., Ebert D. Single-nucleotide polymorphisms of two closely related microsporidian parasites suggest a clonal population expansion after the last glaciation. Mol. Ecol. 2012, 22:314-326.
26. Hatcher M.J., Dunn A.M., Tofts C. The effect of the embryonic bottleneck on vertical microparasite transmission. Computation in Cellular and Molecular Biological Systems 1996, 339-351. World Scientific, Singapore. R. Cuthbertson, M. Holcombe, R. Paton (Eds.).
27. Hatcher M.J., Hogg J.C., Dunn A.M. Local adaptation and enhanced virulence of Nosema granulosis artificially introduced into novel populations of its crustacean host, Gammarus duebeni. Int. J. Parasitol. 2005, 35:265-274.
28. Henzler C.M., Ingólfsson A. The biogeography of the beachflea, Orchestia gammarellus (Crustacea, Amphipoda, Talitridae), in the North Atlantic with special reference to Iceland: a morphometric and genetic study. Zool. Scr. 2008, 37:57-70.
29. Hirt R.P., Logsdon J.M., Healy B., Dorey M.W., Doolittle W.F., Embley T.M. Microsporidia are related to Fungi: evidence from the largest subunit of RNA polymerase II and other proteins. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:580-585.
30. Holmes E.C., Worobey M., Rambaut A. Phylogenetic evidence for recombination in dengue virus. Mol. Biol. Evol. 1999, 16:405-409.
31. Hudson R.R., Boos D.D., Kaplan N.L. A statistical test for detecting geographic subdivision. Mol. Biol. Evol. 1992, 9:138-151.
32. Hugall A., Stanton J., Moritz C. Reticulate evolution and the origins of ribosomal internal transcribed spacer diversity in apomictic Meloidogyne. Mol. Biol. Evol. 1999, 16:157-164.
33. Huson D.H., Bryant D. Application of phylogenetic networks in evolutionary studies. Mol. Biol. Evol. 2006, 23:254-267.
34. Ironside J.E. Multiple losses of sex within a single genus of Microsporidia. BMC Evol. Biol. 2007, 7:48. 10.1186/1471-2148-7-48.
35. Ironside J.E. Diversity and recombination of dispersed ribosomal DNA and protein coding genes in Microsporidia. PLoS One 2013, 8(2):e55878. http://dx.doi.org/10.1371.
36. Ironside J.E., Dunn A.M., Rollinson D., Smith J.E. Association with host mitochondrial haplotypes suggests that feminizing microsporidia lack horizontal transmission. J. Evol. Biol. 2003, 16:1077-1083.
37. Jahnke M., Smith J.E., Dubuffet A., Dunn A.M. Effects of feminizing microsporidia on the masculinizing function of the androgenic gland in Gammarus duebeni. J. Invertebr. Pathol. 2012, 112:146-151.
38. Jobb G., Haeseler A., Strimmer K. TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics. BMC Evol. Biol. 2004, 4:18. 10.1186/1471-2148-4-18.
39. Katoh K., Misawa K., Kuma K., Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002, 30:3059-3066.
40. Keeling P.J., Fast N.M. Microsporidia: biology and evolution of highly reduced intracellular parasites. Annu. Rev. Microbiol. 2002, 56:93-116.
41. Keeling P.J., Luker M.A., Palmer J.D. Evidence from beta-tubulin phylogeny that Microsporidia evolved from within the Fungi. Mol. Biol. Evol. 2000, 17:23-31.
42. Kelly A., Dunn A.M., Hatcher M.J. Incomplete feminisation by the microsporidian sex ratio distorter, Nosema granulosis, and reduced transmission and feminisation efficiency at low temperatures. Int. J. Parasitol. 2002, 32:825-831.
43. Kelly A., Hatcher M.J., Dunn A.M. The impact of a vertically transmitted microsporidian, Nosema granulosis on the fitness of its Gammarus duebeni host under stressful environmental conditions. Parasitology 2003, 126:119-124.
44. Kinne O. Die Gammarus - Arten der Kieler Bucht (G. locusta, G. oceanicus, G. salinus, G. zaddachi, G. duebeni). Zool. Jahrb. (Syst.) 1954, 82:405-424.
45. Knowlton N., Weigt L.A., Solorzano L.A., Mills D.K., Bermingham E. Divergence in proteins, mitochondrial DNA, and reproductive compatibility across the isthmus of Panama. Science 1993, 260:1629-1632.
46. Krebes L., Blank M., Frankowski J., Bastrop R. Molecular characterisation of the Microsporidia of the amphipod Gammarus duebeni across its natural range revealed hidden diversity, wide-ranging prevalence and potential for co-evolution. Infect. Genet. Evol. 2010, 10:1027-1038.
47. Krebes L., Blank M., Jürss K., Zettler M.L., Bastrop R. Glacial-driven vicariance in the amphipod Gammarus duebeni. Mol. Phylogenet. Evol. 2010, 54:372-385.
48. Krebes L., Blank M., Bastrop R. Phylogeography, historical demography and postglacial colonization routes of two amphi-Atlantic distributed amphipods. Syst. Biodivers. 2011, 9:259-273.
49. Lassmann T., Sonnhammer E.L. Kalign-an accurate and fast multiple sequence alignment algorithm. BMC Bioinformatics 2005, 6:298. 10.1186/1471-2105-6-298.
50. Leese F., Kop A., Wägele J.W., Held C. Cryptic speciation in a benthic isopod from Patagonian and Falkland Island waters and the impact of glaciations on its population structure. Front. Zool. 2008, 5:19. 10.1186/1742-9994-5-19.
51. Librado P., Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009, 25:1451-1452.
52. Liu H., Pan G., Song S., Xu J., Li T., Deng Y., Zhou Z. Multiple rDNA units distributed on all chromosomes of Nosema bombycis. J. Invertebr. Pathol. 2008, 99:235-238.
53. Martin D., Rybicki E. RDP: detection of recombination amongst aligned sequences. Bioinformatics 2000, 16:562-563.
54. Martin D.P., Posada D., Crandall K.A., Williamson C. A modified bootscan algorithm for automated identification of recombinant sequences and recombination breakpoints. AIDS Res. Hum. Retroviruses 2005, 21:98-102.
55. Martin D.P., Lemey P., Lott M., Moulton V., Posada D., Lefeuvre P. RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 2010, 26:2462-2463.
56. McTaggart S.J., Dudycha J.L., Omilian A., Crease T.J. Rates of recombination in the ribosomal DNA of apomictically propagated Daphnia obtusa lines. Genetics 2007, 175:311-320.
57. Morgenstern B. DIALIGN: multiple DNA and protein sequence alignment at BiBiServ. Nucleic Acids Res. 2004, 32:W33-W36. (Web Server issue).
58. Morgenstern B., Prohaska S.J., Pöhler D., Stadler P.F. Multiple sequence alignment with user-defined anchor points. Algorithms Mol. Biol. 2006, 1:6. 10.1186/1748-7188-1-6.
59. Müller K. SeqState - primer design and sequence statistics for phylogenetic DNA data sets. Appl. Bioinformatics 2005, 4:65-69.
60. Müller K. Incorporating information from length-mutational events into phylogenetic analysis. Mol. Phylogenet. Evol. 2006, 38:667-676.
61. Nei M. Molecular Evolutionary Genetics 1987, Columbia University Press, New York, USA.
62. Nei M., Li W.H. Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc. Natl. Acad. Sci. U.S.A. 1979, 76:5269-5273.
63. Nei M., Rooney A.P. Concerted and birth-and-death evolution of multigene families. Annu. Rev. Genet. 2005, 39:121-152.
64. Nicholas K.B., Nicholas H.B., Deerfield D.W. GeneDoc: analysis and visualization of genetic variation. Embnew. News 1997, 4:14.
65. Notredame C., Higgins D.G., Heringa J. T-Coffee: a novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 2000, 302:205-217.
66. O'Donnell K., Cigelnik E. Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Mol. Phylogenet. Evol. 1997, 7:103-116.
67. O'Mahony E.M., Tay W.T., Paxton R.J. Multiple rRNA variants in a single spore of the microsporidian Nosema bombi. J. Eukaryot. Microbiol. 2007, 54:103-109.
68. Pacaud A. Les Amphipodes de la faune nutritive des eaux douces francaises. Bull. Franc. Piscic. 1945, 136:105-120.
69. Padidam M., Sawyer S., Fauquet C.M. Possible emergence of new geminiviruses by frequent recombination. Virology 1999, 265:218-225.
70. Parkin E.J., Butlin R.K. Within- and between-individual sequence variation among ITS1 copies in the meadow grasshopper Chorthippus parallelus indicates frequent intrachromosomal gene conversion. Mol. Biol. Evol. 2004, 21:1595-1601.
71. Pillet L., Fontaine D., Pawlowski J. Intra-genomic ribosomal RNA polymorphism and morphological variation in Elphidium macellum suggests inter-specific hybridization in Foraminifera. PLoS One 2012, 7(2):e32373. 10.1371/journal.pone.0032373.
72. Posada D., Crandall K.A. Modeltest: testing the model of DNA substitution. Bioinformatics 1998, 14:817-818.
73. Posada D., Crandall K.A. Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:13757-13762.
74. Reid D.M. On the occurrence of Gammarus duebeni (Lillj.) Crustacea, Amphipoda) in Ireland. Proc. Roy. Irish Acad. B 1939, 45:207-214.
75. Sagastume S., del Aguila C., Martín-Hernández R., Higes M., Henriques-Gil N. Polymorphism and recombination for rDNA in the putatively asexual microsporidian Nosema ceranae, a pathogen of honeybees. Environ. Microbiol. 2011, 13:84-95.
76. Schurko A.M., Neiman M., Logsdon J.M. Signs of sex: what we know and how we know it. Trends Ecol. Evol. 2009, 24:208-217.
77. Sievers F., Wilm A., Dineen D.G., Gibson T.J., Karplus K., Li W., Lopez R., McWilliam H., Remmert M., Söding J., Thompson J.D., Higgins D.G. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 2011, 7:539. 10.1038/msb.2011.75.
78. Smith J.M. Analyzing the mosaic structure of genes. J. Mol. Evol. 1992, 34:126-129.
79. Smith J.E. The ecology and evolution of microsporidian parasites. Parasitology 2009, 136:1901-1914.
80. Subramanian A.R., Kaufmann M., Morgenstern B. DIALIGN-TX: greedy and progressive approaches for segment-based multiple sequence alignment. Algorithms Mol. Biol. 2008, 3:6. 10.1186/1748-7188-3-6.
81. Swofford D.L. PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4 1998, Sinauer Associates, Sunderland, MA, USA.
82. Tamura K., Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 1993, 10:512-526.
83. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28:2731-2739.
84. Terry R.S., Smith J.E., Dunn A.M. Impact of a novel, feminising microsporidium on its crustacean host. J. Eukaryot. Microbiol. 1998, 45:497-501.
85. Terry R.S., Smith J.E., Bouchon D., Rigaud T., Duncanson P., Sharpe R.G., Dunn A.M. Ultrastructural characterisation and molecular taxonomic identification of Nosema granulosis n. sp., a transovarially transmitted feminising (TTF) microsporidium. J. Eukaryot. Microbiol. 1999, 46:492-499.
86. Thompson J.D., Higgins D.G., Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994, 22:4673-4680.
87. Vizoso D.B., Lass S., Ebert D. Different mechanisms of transmission of the microsporidium Octosporea bayeri: a cocktail of solutions for the problem of parasite permanence. Parasitology 2005, 130:1-11.
88. Vossbrinck C.R., Baker M.D., Didier E.S., Debrunner-Vossbrinck B.A., Shadduck J.A. Ribosomal DNA sequences of Encephalitozoon hellem and Encephalitozoon cuniculi: species identification and phylogenetic construction. J. Eukaryot. Microbiol. 1993, 40:354-362.
89. Wallace I.M., O'Sullivan O., Higgins D.G., Notredame C. M-Coffee: combining multiple sequence alignment methods with T-Coffee. Nucleic Acids Res. 2006, 34:1692-1699.
90. Wittner M. Historic perspective on the Microsporidia: expanding horizons. The Microsporidia and Microsporidiosis 1999, 1-6. ASM Press, Washington, DC, USA. M. Wittner, L.M. Weiss (Eds.).
91. Zhu X., Wittner M., Tanowitz H.B., Kotler D., Cali A., Weiss L.M. Small subunit rRNA sequence of Enterocytozoon bieneusi and its potential diagnostic role with use of the polymerase chain reaction. J. Infect. Dis. 1993, 168:1570-1575.