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

TitleMicrosporidia-nematode associations in methane seeps reveal basal fungal parasitism in the deep sea
Publication TypeJournal Article
Year of Publication2014
AuthorsSapir A., Dillman A.R, Connon S.A, Grupe B.M, Ingels J., Mundo-Ocampo M., Levin L.A, Baldwin J.G, Orphan V.J, Sternberg P.W
JournalFrontiers in Microbiology
Date Published2014/02
Type of ArticleArticle
ISBN Number1664-302X
Accession NumberWOS:000331788900001
Keywordsbasal fungi in the deep sea; cold-seep; deep-sea methane seeps; deep-sea microsporidia; diversity; encephalitozoon-cuniculi; evolution; hydrothermal vents; marine; muscle decomposition; nematode; nematodes hosts; parasitism; phylactolaemata; phylogeny; sediment; symbiotic bacteria

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. mansprofundi 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.

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