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Original Research ARTICLE

Front. Microbiol., 10 February 2014 | http://dx.doi.org/10.3389/fmicb.2014.00043

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

  • 1Howard Hughes Medical Institute and Division of Biology, California Institute of Technology, Pasadena, CA, USA
  • 2Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, CA, USA
  • 3Integrative Oceanography Division, Center for Marine Biodiversity and Conservation, Scripps Institution of Oceanography, La Jolla, CA, USA
  • 4Marine Life Support Systems, Plymouth Marine Laboratory, Prospect Place, UK
  • 5Department of Agricultural Biotecnology, Nematology Laboratory, CIIDIR-IPN Unidad Sinaloa, Sinaloa, Mexico
  • 6Department of Nematology, University of California, Riverside, CA, USA

The deep sea is Earth's largest habitat but little is known about the nature of deep-sea parasitism. In contrast to a few characterized cases of bacterial and protistan parasites, the existence and biological significance of deep-sea parasitic fungi is yet to be understood. Here we report the discovery of a fungus-related parasitic microsporidium, Nematocenator marisprofundi n. gen. n. sp. that infects benthic nematodes at methane seeps on the Pacific Ocean floor. This infection is species-specific and has been temporally and spatially stable over 2 years of sampling, indicating an ecologically consistent host-parasite interaction. A high distribution of spores in the reproductive tracts of infected males and females and their absence from host nematodes' intestines suggests a sexual transmission strategy in contrast to the fecal-oral transmission of most microsporidia. N. marisprofundi targets the host's body wall muscles causing cell lysis, and in severe infection even muscle filament degradation. Phylogenetic analyses placed N. marisprofundi in a novel and basal clade not closely related to any described microsporidia clade, suggesting either that microsporidia-nematode parasitism occurred early in microsporidia evolution or that host specialization occurred late in an ancient deep-sea microsporidian lineage. Our findings reveal that methane seeps support complex ecosystems involving interkingdom interactions between bacteria, nematodes, and parasitic fungi and that microsporidia parasitism exists also in the deep-sea biosphere.

Keywords: deep-sea methane seeps, nematodes hosts, deep-sea microsporidia parasitism, muscle decomposition, basal fungi in the deep sea

Citation: Sapir A, Dillman AR, Connon SA, Grupe BM, Ingels J, Mundo-Ocampo M, Levin LA, Baldwin JG, Orphan VJ and Sternberg PW (2014) Microsporidia-nematode associations in methane seeps reveal basal fungal parasitism in the deep sea. Front. Microbiol. 5:43. doi: 10.3389/fmicb.2014.00043

Received: 29 November 2013; Paper pending published: 14 December 2013;
Accepted: 21 January 2014; Published online: 10 February 2014.

Edited by:

Hongyue Dang, Xiamen University, China

Reviewed by:

Catherine Texier, Université Blaise Pascal, France
Ann J. Vanreusel, Ghent University, Belgium

Copyright © 2014 Sapir, Dillman, Connon, Grupe, Ingels, Mundo-Ocampo, Levin, Baldwin, Orphan and Sternberg. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Paul W. Sternberg, Howard Hughes Medical Institute and Division of Biology, California Institute of Technology, 1200 East California Blvd, Pasadena, CA 91125, USA e-mail: pws@caltech.edu

Present address: Adler R. Dillman, Department of Microbiology and Immunology, Stanford University, Stanford, USA