Functional role of phenylacetic acid from metapleural gland secretions in controlling fungal pathogens in evolutionarily derived leaf-cutting ants

Functional role of phenylacetic acid from metapleural gland secretions in controlling fungal pathogens in evolutionarily derived leaf-cutting ants
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DOI:
10.1098/rspb.2015.0212
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发表时间:
2015-05-22
影响因子:
4.7
通讯作者:
Boomsma, Jacobus J.
Boomsma, Jacobus J.
中科院分区:
生物学1区
文献类型:
--
作者:
Fernandez-Marin, Hermogenes;Nash, David R.;Boomsma, Jacobus J.

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种植真菌的蚂蚁群体的大小相差四到五个数量级。他们使用来自放线菌细菌和外分泌腺的化合物作为抗菌剂。ATTA蚁群有数百万只蚂蚁,对于理解卫生策略特别相关,因为它们放弃了祖先对以抗生素为基础的生物防治的主要依赖,转而使用中胸膜腺(MG)化学分泌物。ATTA MGs在合成大量苯乙酸(PAA)方面是独一无二的,苯乙酸是一种已知但研究很少的抗菌剂。我们发现,尤其是最小的工蚁,在积极地将PAA应用于花园碎片中的实验感染目标并将孢子转移到蚂蚁的口腔下腔后,极大地降低了Ecovopsis和绿僵菌孢子的萌发率。体外实验进一步表明,从进化派生的切叶蚂蚁中分离出来的Ecovopsis菌株对PAA的敏感性低于从系统发育上更具基础真菌生长的蚂蚁中分离的菌株,这与Ecovopsis的致病力和控制力之间的进化军备竞赛的动力学一致,但不符合绿僵菌的进化军备竞赛。在几乎完全没有生殖冲突的社会中,Atta蚂蚁形成更大的群体,相对于其他Atta蚂蚁具有更极端的种姓分化。我们假设这些变化与化学害虫管理中独特的进化创新有关,这些创新似乎对专业真菌病原体的抗性选择压力具有很强的抵抗力。
Fungus-farming ant colonies vary four to five orders of magnitude in size. They employ compounds from actinomycete bacteria and exocrine glands as antimicrobial agents. Atta colonies have millions of ants and are particularly relevant for understanding hygienic strategies as they have abandoned their ancestors' prime dependence on antibiotic-based biological control in favour of using metapleural gland (MG) chemical secretions. Atta MGs are unique in synthesizing large quantities of phenylacetic acid (PAA), a known but little investigated antimicrobial agent. We show that particularly the smallest workers greatly reduce germination rates of Escovopsis and Metarhizium spores after actively applying PAA to experimental infection targets in garden fragments and transferring the spores to the ants' infrabuccal cavities. In vitro assays further indicated that Escovopsis strains isolated from evolutionarily derived leaf-cutting ants are less sensitive to PAA than strains from phylogenetically more basal fungus-farming ants, consistent with the dynamics of an evolutionary arms race between virulence and control for Escovopsis, but not Metarhizium. Atta ants form larger colonies with more extreme caste differentiation relative to other attines, in societies characterized by an almost complete absence of reproductive conflicts. We hypothesize that these changes are associated with unique evolutionary innovations in chemical pest management that appear robust against selection pressure for resistance by specialized mycopathogens.