title: Microsporidia-nematode associations in methane seeps reveal basal fungal parasitism in the deep sea.
abstract: 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.
authors.affiliation: Howard Hughes Medical Institute and Division of Biology, California Institute of Technology Pasadena, CA, USA.
authors.forename: Amir
authors.initials: A
authors.lastname: Sapir
authors.affiliation: Howard Hughes Medical Institute and Division of Biology, California Institute of Technology Pasadena, CA, USA.
authors.forename: Adler R
authors.initials: AR
authors.lastname: Dillman
authors.affiliation: Division of Geological and Planetary Sciences, California Institute of Technology Pasadena, CA, USA.
authors.forename: Stephanie A
authors.initials: SA
authors.lastname: Connon
authors.affiliation: Integrative Oceanography Division, Center for Marine Biodiversity and Conservation, Scripps Institution of Oceanography La Jolla, CA, USA.
authors.forename: Benjamin M
authors.initials: BM
authors.lastname: Grupe
authors.affiliation: Marine Life Support Systems, Plymouth Marine Laboratory, Prospect Place UK.
authors.forename: Jeroen
authors.initials: J
authors.lastname: Ingels
authors.affiliation: Department of Agricultural Biotecnology, Nematology Laboratory, CIIDIR-IPN Unidad Sinaloa Sinaloa, Mexico.
authors.forename: Manuel
authors.initials: M
authors.lastname: Mundo-Ocampo
authors.affiliation: Integrative Oceanography Division, Center for Marine Biodiversity and Conservation, Scripps Institution of Oceanography La Jolla, CA, USA.
authors.forename: Lisa A
authors.initials: LA
authors.lastname: Levin
authors.affiliation: Department of Nematology, University of California Riverside, CA, USA.
authors.forename: James G
authors.initials: JG
authors.lastname: Baldwin
authors.affiliation: Division of Geological and Planetary Sciences, California Institute of Technology Pasadena, CA, USA.
authors.forename: Victoria J
authors.initials: VJ
authors.lastname: Orphan
authors.affiliation: Howard Hughes Medical Institute and Division of Biology, California Institute of Technology Pasadena, CA, USA.
authors.forename: Paul W
authors.initials: PW
authors.lastname: Sternberg
keywords: basal fungi in the deep sea; deep-sea methane seeps; deep-sea microsporidia parasitism; muscle decomposition; nematodes hosts