Microsporidia-nematode associations in methane seeps reveal basal fungal parasitism in the deep sea

Frontiers in Microbiology

Volumn 5, Issue FEB, 2014, Pages

  Sapir, Amir ^a   Dillman, Adler R ^a,g   Connon, Stephanie A ^b   Grupe, Benjamin M ^c   Ingels, Jeroen ^d   Mundo Ocampo, Manuel ^e   Levin, Lisa A ^c   Baldwin, James G ^f   Orphan, Victoria J ^b   Sternberg, Paul W ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^c INTEGRATIVE OCEANOGRAPHY DIVISION   (United States)

^d PLYMOUTH MARINE LABORATORY   (United Kingdom)

^e INSTITUTO POLITÉCNICO NACIONAL   (Mexico)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g STANFORD UNIVERSITY   (United States)

Author keywords

Basal fungi in the deep sea; Deep sea methane seeps; Deep sea microsporidia parasitism; Muscle decomposition; Nematodes hosts

Indexed keywords

ADULT; ARTICLE; CONTROLLED STUDY; CYTOLYSIS; DEEP SEA; DESMODORA; FEMALE; FUNGAL STRUCTURES; FUNGUS SPORE; HOST PARASITE INTERACTION; IN SITU HYBRIDIZATION; MALE; MICROSPORIDIA; MYCOPARASITISM; NEMATOCENATOR MARISPROFUNDI; NEMATODE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PROCHAETOSOMA; SCANNING ELECTRON MICROSCOPY; SEXUAL TRANSMISSION;

EID: 84897652252     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00043     Document Type: Article

References (59)

1. Abdel-Ghaffar, F., Bashtar, A. R., Mehlhorn, H., Al-Rasheid, K., and Morsy, K. (2011). Microsporidian parasites: a danger facing marine fishes of the Red Sea. Parasitol. Res. 108, 219-225. doi: 10.1007/s00436-010-2061-1
2. Adams, B. J., Wall, D. H., Gozel, U., Dillman, A. R., Chaston, J. M., and Hogg, I. D. (2007). The southernmost worm, Scottnema lindsayae (Nematoda): diversity, dispersal and ecological stability. Polar Biol. 30, 809-815. doi: 10.1007/s00300-006-0241-3
3. Ardila-Garcia, A. M., and Fast, N. M. (2012). Microsporidian infection in a free-living marine nematode. Eukaryot. Cell 11, 1544-1551. doi: 10.1128/Ec.00228-12
4. Bass, D., Howe, A., Brown, N., Barton, H., Demidova, M., Michelle, H., et al. (2007). Yeast forms dominate fungal diversity in the deep oceans. Proc. Biol. Sci. 274, 3069-3077. doi: 10.1098/rspb.2007.1067
5. Becnel, J. J., Hazard, E. I., Fukuda, T., and Sprague, V. (1987). Life-Cycle of Culicospora-magna (Kudo, 1920) (Microsporida, Culicosporidae) in Culex-restuans Theobald with Special Reference to Sexuality. J. Protozool. 34, 313-322. doi: 10.1111/j.1550-7408.1987.tb03182.x
6. Borgonie, G., Garcia-Moyano, A., Litthauer, D., Bert, W., Bester, A., Van Heerden, E., et al. (2011). Nematoda from the terrestrial deep subsurface of South Africa. Nature 474, 79-82. doi: 10.1038/Nature09974
7. Bulgheresi, S., Gruber-Vodicka, H. R., Heindl, N. R., Dirks, U., Kostadinova, M., Breiteneder, H., et al. (2011). Sequence variability of the pattern recognition receptor Mermaid mediates specificity of marine nematode symbioses. ISME J. 5, 986-998. doi: 10.1038/ismej.2010.198
8. Burgaud, G., Arzur, D., Sampaio, J. P., and Barbier, G. (2011). Candida oceani sp nov., a novel yeast isolated from a Mid-Atlantic Ridge hydrothermal vent (-2300 meters). Antonie Van Leeuwenhoek 100, 75-82. doi: 10.1007/s10482-011-9566-1
9. Burgaud, G., Le Calvez, T., Arzur, D., Vandenkoornhuyse, P., and Barbier, G. (2009). Diversity of culturable marine filamentous fungi from deep-sea hydrothermal vents. Environ. Microbiol. 11, 1588-1600. doi: 10.1111/j.1462-2920.2009.01886.x
10. Burri, L., Williams, B. A., Bursac, D., Lithgow, T., and Keeling, P. J. (2006). Microsporidian mitosomes retain elements of the general mitochondrial targeting system. Proc. Natl. Acad. Sci. U.S.A. 103, 15916-15920. doi: 10.1073/pnas.0604109103
11. Canning, E. U., Refardt, D., Vossbrinck, C. R., Okamura, B., and Curry, A. (2002). New diplokaryotic microsporidia (Phylum Microsporidia) from freshwater bryozoans (Bryozoa, Phylactolaemata). Eur. J. Protistol. 38, 247-265. doi: 10.1078/0932-4739-00867
12. Capella-Gutierrez, S., Marcet-Houben, M., and Gabaldon, T. (2012). Phylogenomics supports microsporidia as the earliest diverging clade of sequenced fungi. BMC Biol. 10:47. doi: 10.1186/1741-7007-10-47
13. Cuomo, C. A., Desjardins, C. A., Bakowski, M. A., Goldberg, J., Ma, A. T., Becnel, J. J., et al. (2012). Microsporidian genome analysis reveals evolutionary strategies for obligate intracellular growth. Genome Res. 22, 2478-2488. doi: 10.1101/gr.142802.112
14. Deprez, T., Steyaert, M., Vanaverbeke, J., Speybroeck, J., Raes, M., Derycke, S., et al. (2005). NeMys. World Wide Web Electronic Publication. Department of Marine Biology, Ghent University. Available online at: http://www.nemys.ugent.be
15. Dubina, V. R., and Isakov, L. S. (1976). New species of Microsporidia from the gallbladder of deep-sea fishes. Parazitologiia 10, 556-560.
16. Estes, K. A., Szumowski, S. C., and Troemel, E. R. (2011). Non-lytic, actin-based exit of intracellular parasites from C. elegans intestinal cells. PLoS Pathog. 7:e1002227. doi: 10.1371/journal.ppat.1002227
17. Felix, M. A., and Braendle, C. (2010). The natural history of Caenorhabditis elegans. Curr. Biol. 20, R965-R969. doi: 10.1016/j.cub.2010.09.050
18. Ghosh, K., and Weiss, L. M. (2009). Molecular diagnostic tests for microsporidia. Interdiscip. Perspect. Infect. Dis. 2009, 926521. doi: 10.1155/2009/926521
19. Goertz, D., and Hoch, G. (2011). Modeling horizontal transmission of microsporidia infecting gypsy moth, Lymantria dispar (L.), larvae. Biol. Control 56, 263-270. doi: 10.1016/j.biocontrol.2010.11.013
20. Guilini, K., Levin, L. A., and Vanreusel, A. (2012). Cold seep and oxygen minimum zone associated sources of margin heterogeneity affect benthic assemblages, diversity and nutrition at the Cascadian margin (NE Pacific Ocean). Prog. Oceanogr. 96, 77-92. doi: 10.1016/j.pocean.2011.10.003
21. Holterman, M., Van Der Wurff, A., Van Den Elsen, S., Van Megen, H., Bongers, T., Holovachov, O., et al. (2006). Phylum-wide analysis of SSU rDNA reveals deep phylogenetic relationships among nematodes and accelerated evolution toward crown clades. Mol. Biol. Evol. 23, 1792-1800. doi: 10.1093/molbev/mls044
22. Ingels, J., Tchesunov, A. V., and Vanreusel, A. (2011). Meiofauna in the Gollum Channels and the Whittard Canyon, Celtic Margin-how local environmental conditions shape nematode structure and function. PLoS ONE 6:e20094. doi: 10.1371/journal.pone.0020094
23. James, T. Y., Kauff, F., Schoch, C. L., Matheny, P. B., Hofstetter, V., Cox, C. J., et al. (2006). Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443, 818-822. doi: 10.1038/Nature05110
24. Jones, E. B. G. (2011). Are there more marine fungi to be described? Botanica Marina 54, 343-354. doi: 10.1515/Bot.2011.043
25. Katinka, M. D., Duprat, S., Cornillot, E., Metenier, G., Thomarat, F., Prensier, G., et al. (2001). Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 414, 450-453. doi: 10.1038/35106579
26. Keeling, P. J., and Fast, N. M. (2002). Microsporidia: biology and evolution of highly reduced intracellular parasites. Annu. Rev. Microbiol. 56, 93-116. doi: 10.1146/annurev.micro.56.012302.160854
27. Keeling, P. J., Fast, N. M., Law, J. S., Williams, B. A., and Slamovits, C. H. (2005). Comparative genomics of microsporidia. Folia Parasitol. 52, 8-14. doi: 10.14411/fp.2005.002
28. Knittel, K., and Boetius, A. (2009). Anaerobic oxidation of methane: progress with an unknown process. Annu. Rev. Microbiol. 63, 311-334. doi: 10.1146/annurev.micro.61.080706.093130
29. Lacey, L. A., Frutos, R., Kaya, H. K., and Vail, P. (2001). Insect pathogens as biological control agents: do they have a future? Biol. Control 21, 230-248. doi: 10.1006/bcon.2001.0938
30. Lewthwaite, P., Gill, G. V., Hart, C. A., and Beeching, N. J. (2005). Gastrointestinal parasites in the immunocompromised. Curr. Opin. Infect. Dis. 18, 427-435. doi: 10.1097/01.qco.0000182104.40128.18
31. Lopez-Garcia, P., Philippe, H., Gail, F., and Moreira, D. (2003). Autochthonous eukaryotic diversity in hydrothermal sediment and experimental microcolonizers at the Mid-Atlantic Ridge. Proc. Natl. Acad. Sci. U.S.A. 100, 697-702. doi: 10.1073/pnas.0235779100
32. Martin, W., Baross, J., Kelley, D., and Russell, M. J. (2008). Hydrothermal vents and the origin of life. Nat. Rev. Microbiol. 6, 805-814. doi: 10.1038/Nrmicro1991
33. McMullin, E. R., Bergquist, D. C., and Fisher, C. R. (2000). Metazoans in extreme environments: adaptations of hydrothermal vent and hydrocarbon seep fauna. Gravit. Space Biol. Bull. 13, 13-23.
34. Moreira, D., and Lopez-Garcia, P. (2003). Are hydrothermal vents oases for parasitic protists? Trends Parasitol. 19, 556-558. doi: 10.1016/j.pt.2003.09.013
35. Morris, D. J., Terry, R. S., and Adams, A. (2005). Development and molecular characterisation of the microsporidian Schroedera airthreyi n. sp in a freshwater bryozoan Plumatella sp (Bryozoa: Phylactolaemata). J. Eukaryot. Microbiol. 52, 31-37. doi: 10.1111/j.1550-7408.2005.3283r.x
36. Musat, N., Giere, O., Gieseke, A., Thiermann, F., Amann, R., and Dubilier, N. (2007). Molecular and morphological characterization of the association between bacterial endosymbionts and the marine nematode Astomonema sp from the Bahamas. Environ. Microbiol. 9, 1345-1353. doi: 10.1111/j.1462-2920.2006.01232.x
37. Nagahama, T., Hamamoto, M., Nakase, T., and Horikoshi, K. (2003). Rhodotorula benthica sp nov and Rhodotorula calyptogenae sp nov., novel yeast species from animals collected from the deep-sea floor, and Rhodotorula lysiniphila sp nov., which is related phylogenetically. Int. J. Syst. Evol. Microbiol. 53, 897-903. doi: 10.1099/ijs.0.02395-0
38. Nagahama, T., Takahashi, E., Nagano, Y., Abdel-Wahab, M. A., and Miyazaki, M. (2011). Molecular evidence that deep-branching fungi are major fungal components in deep-sea methane cold-seep sediments. Environ. Microbiol. 13, 2359-2370. doi: 10.1111/j.1462-2920.2011.02507.x
39. Pawlowski, J., Christen, R., Lecroq, B., Bachar, D., Shahbazkia, H. R., Amaral-Zettler, L., et al. (2011). Eukaryotic richness in the abyss: insights from pyrotag sequencing. PLoS ONE 6:e18169. doi: 10.1371/journal.pone.0018169
40. Platt, H. M., and Warwick, R. (1988). Free-living Marine Nematodes. Part II. British Chromadorids: Pictorial Key to World Genera and Notes for the Identification of British Species. Leiden: E.J. Brill, W. Backhuys, 264.
41. Polz, M. F., Felbeck, H., Novak, R., Nebelsick, M., and Ott, J. A. (1992). Chemoautotrophic, sulfur-oxidizing symbiotic bacteria on marine nematodes-morphological and biochemical-characterization. Microb. Ecol. 24, 313-329. doi: 10.1007/Bf00167789
42. Porter, S. D., Valles, S. M., Davis, T. S., Briano, J. A., Calcaterra, L. A., Oi, D. H., et al. (2007). Host specificity of the microsporidian pathogen Vairimorpha iivvictae at five field sites with infected Solenopsis invicta fire ant colonies in northern Argentina. Fla. Entomol. 90, 447-452. doi: 10.1653/0015-4040(2007)90[447:HSOTMP]2.0.CO;2
43. Sibuet, M., and Olu, K. (1998). Biogeography, biodiversity and fluid dependence of deep-sea cold-seep communities at active and passive margins. Deep-Sea Res. Part II Top. Stud. Oceanogr. 45, 517-567. doi: 10.1016/S0967-0645(97)00074-X
44. Somerfield, P. J., and Warwick, R. M. (1996). Meiofauna in Marine Pollution Monitoring Programmes: A Laboratory Manual. Lowestoft: MAFF.
45. Takishita, K., Yubuki, N., Kakizoe, N., Inagaki, Y., and Maruyama, T. (2007). Diversity of microbial eukaryotes in sediment at a deep-sea methane cold seep: surveys of ribosomal DNA libraries from raw sediment samples and two enrichment cultures. Extremophiles 11, 563-576. doi: 10.1007/s00792-007-0068-z
46. Tchesunov, A. V., Ingels, J., and Popova, E. V. (2012). Marine free-living nematodes associated with symbiotic bacteria in deep-sea canyons of north-east Atlantic Ocean. J. Marine Biol. Assoc. U. K. 92, 1257-1271. doi: 10.1017/S0025315411002116
47. Terry, R. S., Dunn, A. M., and Smith, J. E. (1997). Cellular distribution of a feminizing microsporidian parasite: a strategy for transovarial transmission. Parasitology 115, 157-163. doi: 10.1017/S0031182097001236
48. Texier, C., Vidau, C., Vigues, B., El Alaoui, H., and Delbac, F. (2010). Microsporidia: a model for minimal parasite-host interactions. Curr. Opin. Microbiol. 13, 443-449. doi: 10.1016/j.mib.2010.05.005
49. Thaler, A. D., Van Dover, C. L., and Vilgalys, R. (2012). Ascomycete phylotypes recovered from a Gulf of Mexico methane seep are identical to an uncultured deep-sea fungal clade from the Pacific. Fungal Ecol. 5, 270-273. doi: 10.1016/j.funeco.2011.07.002
50. Thurber, A. R., Levin, L. A., Orphan, V. J., and Marlow, J. J. (2012). Archaea in metazoan diets: implications for food webs and biogeochemical cycling. ISME J. 6, 1602-1612. doi: 10.1038/ismej.2012.16
51. Troemel, E. R., Felix, M. A., Whiteman, N. K., Barriere, A., and Ausubel, F. M. (2008). Microsporidia are natural intracellular parasites of the nematode Caenorhabditis elegans. PLoS Biol. 6, 2736-2752. doi: 10.1371/journal.pbio.0060309
52. Tsaousis, A. D., Kunji, E. R. S., Goldberg, A. V., Lucocq, J. M., Hirt, R. P., and Embley, T. M. (2008). A novel route for ATP acquisition by the remnant mitochondria of Encephalitozoon cuniculi. Nature 453, 553-556. doi: 10.1038/Nature06903
53. Van Dover, C. L., Ward, M. E., Scott, J. L., Underdown, J., Anderson, B., Gustafson, C., et al. (2007). A fungal epizootic in mussels at a deep-sea hydrothermal vent. Mar. Ecol. Evol. Perspect. 28, 54-62. doi: 10.1111/j.1439-0485.2006.00121.x
54. Vanreusel, A., De Groote, A., Gollner, S., and Bright, M. (2010a). Ecology and biogeography of free-living nematodes associated with chemosynthetic environments in the deep sea: a review. PLoS ONE 5:e12449. doi: 10.1371/journal.pone.0012449
55. Vanreusel, A., Fonseca, G., Danovaro, R., Da Silva, M. C., Esteves, A. M., Ferrero, T., et al. (2010b). The contribution of deep-sea macrohabitat heterogeneity to global nematode diversity. Mar. Ecol. Evol. Perspect. 31, 6-20. doi: 10.1111/j.1439-0485.2009.00352.x
56. Vavra, J., and Larsson, J. I. R. (1999). Structure of the Microsporidia. Washington, D.C: Amer Society for Microbiology press.
57. Verschelde, D., Gourbault, N., and Vincx, M. (1998). Revision of Desmodora with descriptions of new desmodorids (Nematoda) from hydrothermal vents of the Pacific. J. Mar. Biol. Assoc. U.K. 78, 75-112. doi: 10.1017/S0025315400039977
58. Vossbrinck, C. R., and Debrunner-Vossbrinck, B. A. (2005). Molecular phylogeny of the Microsporidia: ecological, ultrastructural and taxonomic considerations. Folia Parasitol (Praha) 52, 131-142; discussion 130. doi: 10.14411/fp.2005.017
59. Xu, Y., and Weiss, L. M. (2005). The microsporidian polar tube: a highly specialised invasion organelle. Int. J. Parasitol. 35, 941-953. doi: 10.1016/j.ijpara.2005.04.003