Variation in Pseudonocardia antibiotic defence helps govern parasite-induced morbidity in Acromyrmex leaf-cutting ants

被引:72
作者
Poulsen, Michael [1 ]
Cafaro, Matias J. [1 ,3 ]
Erhardt, Daniel P. [1 ]
Little, Ainslie E. F. [1 ]
Gerardo, Nicole M. [4 ]
Tebbets, Brad [2 ]
Klein, Bruce S. [2 ]
Currie, Cameron R. [1 ]
机构
[1] Univ Wisconsin, Dept Bacteriol, Madison, WI 53706 USA
[2] Univ Wisconsin, Dept Med Microbiol & Immunol, Madison, WI 53706 USA
[3] Univ Puerto Rico, Dept Biol, Mayaguez, PR 00681 USA
[4] Emory Univ, Dept Biol, O Wayne Rollins Res Ctr, Atlanta, GA 30322 USA
来源
ENVIRONMENTAL MICROBIOLOGY REPORTS | 2010年 / 2卷 / 04期
基金
美国国家科学基金会;
关键词
FUNGUS-GROWING ANTS; ACTINOMYCETE BACTERIA; COEVOLUTION; PROTECT; GARDEN; EVOLUTION; SYMBIOSIS; HISTORY; GLANDS;
D O I
10.1111/j.1758-2229.2009.00098.x
中图分类号
X [环境科学、安全科学];
学科分类号
08 ; 0830 ;
摘要
P>Host-parasite associations are potentially shaped by evolutionary reciprocal selection dynamics, in which parasites evolve to overcome host defences and hosts are selected to counteract these through the evolution of new defences. This is expected to result in variation in parasite-defence interactions, and the evolution of resistant parasites causing increased virulence. Fungus-growing ants maintain antibiotic-producing Pseudonocardia (Actinobacteria) that aid in protection against specialized parasites of the ants' fungal gardens, and current evidence indicates that both symbionts have been associated with the ants for millions of years. Here we examine the extent of variation in the defensive capabilities of the ant-actinobacterial association against Escovopsis (parasite-defence interactions), and evaluate how variation impacts colonies of fungus-growing ants. We focus on five species of Acromyrmex leaf-cutting ants, crossing 12 strains of Pseudonocardia with 12 strains of Escovopsis in a Petri plate bioassay experiment, and subsequently conduct subcolony infection experiments using resistant and non-resistant parasite strains. Diversity in parasite-defence interactions, including pairings where the parasites are resistant, suggests that chemical variation in the antibiotics produced by different actinobacterial strains are responsible for the observed variation in parasite susceptibility. We evaluate the role this variation plays showing that infection of ant subcolonies with resistant parasite strains results in significantly higher parasite-induced morbidity with respect to garden biomass loss. Our findings thus further establish the role of Pseudonocardia-derived antibiotics in helping defend the ants' fungus garden from the parasite Escovopsis, and provide evidence that small molecules can play important roles as antibiotics in a natural system.
引用
收藏
页码:534 / 540
页数:7
相关论文
共 46 条
[1]  
Bot ANM, 2001, EVOLUTION, V55, P1980, DOI 10.1111/j.0014-3820.2001.tb01315.x
[2]   Variable sensitivity of fungi and bacteria to compounds produced by the metapleural glands of leaf-cutting ants [J].
Bot, ANM ;
Ortius-Lechner, D ;
Finster, K ;
Maile, R ;
Boomsma, JJ .
INSECTES SOCIAUX, 2002, 49 (04) :363-370
[3]   Phylogenetic analysis of mutualistic filamentous bacteria associated with fungus-growing ants [J].
Cafaro, MJ ;
Currie, CR .
CANADIAN JOURNAL OF MICROBIOLOGY, 2005, 51 (06) :441-446
[4]   Insect Symbioses: A Case Study of Past, Present, and Future Fungus-growing Ant Research [J].
Caldera, Eric J. ;
Poulsen, Michael ;
Suen, Garret ;
Currie, Cameron R. .
ENVIRONMENTAL ENTOMOLOGY, 2009, 38 (01) :78-92
[5]   EVOLUTIONARY HISTORY OF THE SYMBIOSIS BETWEEN FUNGUS-GROWING ANTS AND THEIR FUNGI [J].
CHAPELA, IH ;
REHNER, SA ;
SCHULTZ, TR ;
MUELLER, UG .
SCIENCE, 1994, 266 (5191) :1691-1694
[6]   The natural history of antibiotics [J].
Clardy, Jon ;
Fischbach, Michael A. ;
Currie, Cameron R. .
CURRENT BIOLOGY, 2009, 19 (11) :R437-R441
[7]   New antibiotics from bacterial natural products [J].
Clardy, Jon ;
Fischbach, Michael A. ;
Walsh, Christopher T. .
NATURE BIOTECHNOLOGY, 2006, 24 (12) :1541-1550
[8]   Changing patterns of infectious disease [J].
Cohen, ML .
NATURE, 2000, 406 (6797) :762-767
[9]   Coevolved crypts and exocrine glands support mutualistic bacteria in fungus-growing ants [J].
Currie, CR ;
Poulsen, M ;
Mendenhall, J ;
Boomsma, JJ ;
Billen, J .
SCIENCE, 2006, 311 (5757) :81-83
[10]   Fungus-growing ants use antibiotic-producing bacteria to control garden parasites [J].
Currie, CR ;
Scott, JA ;
Summerbell, RC ;
Malloch, D .
NATURE, 1999, 398 (6729) :701-704