Microsporidia Are Natural Intracellular Parasites of the Nematode Caenorhabditis elegans

被引:184
作者
Troemel, Emily R. [1 ,2 ]
Felix, Marie-Anne [3 ,4 ]
Whiteman, Noah K. [5 ]
Barriere, Antoine [3 ,4 ]
Ausubel, Frederick M. [1 ,2 ]
机构
[1] Harvard Univ, Sch Med, Dept Genet, Dept Mol Biol, Boston, MA USA
[2] Massachusetts Gen Hosp, Ctr Computat & Integrat Biol, Boston, MA 02114 USA
[3] Univ Paris 06, CNRS, Inst Jacques Monod, Paris, France
[4] Univ Paris 07, Inst Jacques Monod, CNRS, F-75251 Paris, France
[5] Harvard Univ, Dept Organism & Evolutionary Biol, Cambridge, MA 02138 USA
基金
美国国家卫生研究院;
关键词
D O I
10.1371/journal.pbio.0060309
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
For decades the soil nematode Caenorhabditis elegans has been an important model system for biology, but little is known about its natural ecology. Recently, C. elegans has become the focus of studies of innate immunity and several pathogens have been shown to cause lethal intestinal infections in C. elegans. However none of these pathogens has been shown to invade nematode intestinal cells, and no pathogen has been isolated from wild-caught C. elegans. Here we describe an intracellular pathogen isolated from wild-caught C. elegans that we show is a new species of microsporidia. Microsporidia comprise a large class of eukaryotic intracellular parasites that are medically and agriculturally important, but poorly understood. We show that microsporidian infection of the C. elegans intestine proceeds through distinct stages and is transmitted horizontally. Disruption of a conserved cytoskeletal structure in the intestine called the terminal web correlates with the release of microsporidian spores from infected cells, and appears to be part of a novel mechanism by which intracellular pathogens exit from infected cells. Unlike in bacterial intestinal infections, the p38 MAPK and insulin/insulin-like growth factor (IGF) signaling pathways do not appear to play substantial roles in resistance to microsporidian infection in C. elegans. We found microsporidia in multiple wild-caught isolates of Caenorhabditis nematodes from diverse geographic locations. These results indicate that microsporidia are common parasites of C. elegans in the wild. In addition, the interaction between C. elegans and its natural microsporidian parasites provides a system in which to dissect intracellular intestinal infection in vivo and insight into the diversity of pathogenic mechanisms used by intracellular microbes.
引用
收藏
页码:2736 / 2752
页数:17
相关论文
共 68 条
[31]   A higher-level phylogenetic classification of the Fungi [J].
Hibbett, David S. ;
Binder, Manfred ;
Bischoff, Joseph F. ;
Blackwell, Meredith ;
Cannon, Paul F. ;
Eriksson, Ove E. ;
Huhndorf, Sabine ;
James, Timothy ;
Kirk, Paul M. ;
Luecking, Robert ;
Lumbsch, H. Thorsten ;
Lutzoni, Francois ;
Matheny, P. Brandon ;
Mclaughlin, David J. ;
Powell, Martha J. ;
Redhead, Scott ;
Schoch, Conrad L. ;
Spatafora, Joseph W. ;
Stalpers, Joost A. ;
Vilgalys, Rytas ;
Aime, M. Catherine ;
Aptroot, Andre ;
Bauer, Robert ;
Begerow, Dominik ;
Benny, Gerald L. ;
Castlebury, Lisa A. ;
Crous, Pedro W. ;
Dai, Yu-Cheng ;
Gams, Walter ;
Geiser, David M. ;
Griffith, Gareth W. ;
Gueidan, Cecile ;
Hawksworth, David L. ;
Hestmark, Geir ;
Hosaka, Kentaro ;
Humber, Richard A. ;
Hyde, Kevin D. ;
Ironside, Joseph E. ;
Koljalg, Urmas ;
Kurtzman, Cletus P. ;
Larsson, Karl-Henrik ;
Lichtwardt, Robert ;
Longcore, Joyce ;
Miadlikowska, Jolanta ;
Miller, Andrew ;
Moncalvo, Jean-Marc ;
Mozley-Standridge, Sharon ;
Oberwinkler, Franz ;
Parmasto, Erast ;
Reeb, Valerie .
MYCOLOGICAL RESEARCH, 2007, 111 :509-547
[32]   Evaluation of universal probes and primer sets for assessing total bacterial load in clinical samples: General implications and practical use in endodontic antimicrobial therapy [J].
Horz, HP ;
Vianna, ME ;
Gomes, BPFA ;
Conrads, G .
JOURNAL OF CLINICAL MICROBIOLOGY, 2005, 43 (10) :5332-5337
[33]   MRBAYES: Bayesian inference of phylogenetic trees [J].
Huelsenbeck, JP ;
Ronquist, F .
BIOINFORMATICS, 2001, 17 (08) :754-755
[34]   PAMP recognition and the plant-pathogen arms race [J].
Ingle, Robert A. ;
Carstens, Maryke ;
Denby, Katherine J. .
BIOESSAYS, 2006, 28 (09) :880-889
[35]   Role for β-catenin and HOX transcription factors in Caenorhabditis elegans and mammalian host epithelial-pathogen interactions [J].
Irazoqui, Javier E. ;
Ng, Aylwin ;
Xavier, Ramnik J. ;
Ausubel, Frederick M. .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2008, 105 (45) :17469-17474
[36]   Plant innate immunity - direct and indirect recognition of general and specific pathogen-associated molecules [J].
Jones, DA ;
Takemoto, D .
CURRENT OPINION IN IMMUNOLOGY, 2004, 16 (01) :48-62
[37]   The plant immune system [J].
Jones, Jonathan D. G. ;
Dangl, Jeffery L. .
NATURE, 2006, 444 (7117) :323-329
[38]   Interaction of bacterial pathogens with polarized epithelium [J].
Kazmierczak, BI ;
Mostov, K ;
Engel, JN .
ANNUAL REVIEW OF MICROBIOLOGY, 2001, 55 :407-435
[39]   Microsporidia: Biology and evolution of highly reduced intracellular parasites [J].
Keeling, PJ ;
Fast, NM .
ANNUAL REVIEW OF MICROBIOLOGY, 2002, 56 :93-116
[40]  
KEOHANE EM, 1999, MICROSPORIDIA MICROS