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

Sapir, Amir and Dillman, Adler R. and Connon, Stephanie A. and Grupe, Benjamin M. and Ingels, Jeroen and Mundo-Ocampo, Manuel and Levin, Lisa A. and Baldwin, James G. and Orphan, Victoria J. and Sternberg, Paul W. (2014) Microsporidia-nematode associations in methane seeps reveal basal fungal parasitism in the deep sea. Frontiers in Microbiology, 5 . Art. No. 43. ISSN 1664-302X. PMCID PMC3918590. https://resolver.caltech.edu/CaltechAUTHORS:20140310-102130554

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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.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://journal.frontiersin.org/Journal/10.3389/fmicb.2014.00043/abstractPublisherArticle
http://dx.doi.org/10.3389/fmicb.2014.00043DOIArticle
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3918590/PubMed CentralArticle
ORCID:
AuthorORCID
Sapir, Amir0000-0001-9888-1800
Dillman, Adler R.0000-0001-7171-4332
Grupe, Benjamin M.0000-0002-5421-7278
Ingels, Jeroen0000-0001-8342-2222
Levin, Lisa A.0000-0002-2858-8622
Baldwin, James G.0000-0001-6468-0285
Orphan, Victoria J.0000-0002-5374-6178
Sternberg, Paul W.0000-0002-7699-0173
Additional Information:© 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. Received: 29 November 2013; Paper pending published: 14 December 2013; Accepted: 21 January 2014; Published online: 10 February 2014. We thank captain, crew, Alvin and Jason II pilots, and cruise participants of Atlantis legs 15-68 and 18-10 for assistance with sample collection. We thank Alasdair McDowall for excellent TEM assistance, Nathalie De Hauwere and the Flanders Marine Institute for drawing the HR map, Stephen Meisenhelter for worm picking, Emily Troemel for sharing reagents, John Curington for Latin grammar advice, Katja Guilini for sharing samples, slides, published data about HR nematodes, James Becnel for comments on the manuscript, and Greg Rouse for E4 rock photo. This work was supported by the Howard Hughes Medical Institute, with which PWS is an investigator, sample collection was supported by NSF OCE 0826254 to LAL and NSF OCE-0825791 to VJO, and an NIH USPHS Training Grant (T32GM07616) to A.R.D. JI is supported by a Marie Curie Intra-European Fellowship within the 7th European Community Framework Programme (Grant Agreement FP7-PEOPLE-2011-IEF No 300879). Running title: Microsporidia parasitism in deep-sea methane seeps
Funders:
Funding AgencyGrant Number
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
NSFOCE 0826254
NSFOCE-0825791
NIHT32GM07616
Marie Curie Fellowship300879
Subject Keywords:deep-sea methane seeps, nematodes hosts, deep-sea microsporidia parasitism, muscle decomposition, basal fungi in the deep sea
PubMed Central ID:PMC3918590
Record Number:CaltechAUTHORS:20140310-102130554
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20140310-102130554
Official 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 - See more at: http://journal.frontiersin.org/Journal/10.3389/fmicb.2014.00043/abstract#sthash.ieAqSVG7.dpuf
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:44218
Collection:CaltechAUTHORS
Deposited By: Ruth Sustaita
Deposited On:10 Mar 2014 18:17
Last Modified:03 Oct 2019 06:15

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