28 minutes later: investigating the role of aflatrem-like compounds in Ophiocordyceps parasite manipulation of zombie ants

28 minutes later: investigating the role of aflatrem-like compounds in Ophiocordyceps parasite manipulation of zombie ants
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DOI:
10.1016/j.anbehav.2023.06.011
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发表时间:
2023-08-23
期刊:
影响因子:
2.5
通讯作者:
de Bekker, Charissa
de Bekker, Charissa
中科院分区:
生物学2区
文献类型:
--
作者:
Beckerson, William C.;Krider, Courtney;de Bekker, Charissa

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寄生虫和它们的宿主之间的共同进化关系可以导致随着时间的推移出现不同的表型,如在操纵昆虫和蜘蛛行为以帮助真菌孢子传播的Ophiocorphic真菌中所见。最明显的例子是Camponotini部落的蚂蚁,俗称“僵尸蚂蚁”。虽然在感染过程中诱导的行为得到了很好的描述,但其分子基础仍然未知。最近的基因组学和转录组学分析的camponoti-floridani已经确定了几个高度上调的生物分子产生的真菌感染的Camponotus floridanus。其中有一种麦角生物碱与真菌毒素黄曲霉素有关,已知黄曲霉素会引起奶牛的“蹒跚综合征”。交错,定义为不稳定的运动侧到侧,也观察到在C。floridanus蚂蚁在后期感染。为了测试是否aflatrem类化合物可以负责,我们用aflatrem注射健康蚂蚁,并记录他们的行为30分钟。使用自动对象跟踪软件MARGO和手动行为量化,我们发现aflatrem减少蚂蚁的活动和速度,并增加惊人的行为。为了研究潜在的转录组学变化,我们对注射黄曲霉素的蚂蚁的头部进行了RNA-seq,与之前对Ophiocordycepsmanipulated蚂蚁的转录组学工作保持一致。我们确定了261个基因,与假注射对照相比,在注射黄曲霉素的蚂蚁中显著失调。当与来自Ophiocordycepsmanipulated蚂蚁的RNA-seq数据比较时,我们发现两组共有113个差异调节基因。这些基因包括感觉神经元膜蛋白基因、几种气味结合蛋白基因和肌肉骨骼基因,如肌联蛋白和暗蛋白。总之,这些结果表明,黄曲霉素样化合物显着影响C。floridanus C. floridanus和Bos taurus认为,在整个生命之树中展示的行为操纵策略可能在方法上更相似,如果不是在应用上有很大差异的话,比我们意识到的要多。(c)2023作者(S)由Elsevier Ltd代表动物行为研究协会出版。这是CC BY许可证下的开放获取文章(http:creativecommons.org/licenses/ by/4.0/)。
Coevolutionary relationships between parasites and their hosts can lead to the emergence of diverse phenotypes over time, as seen in Ophiocordyceps fungi that manipulate insect and arachnid behaviour to aid fungal spore transmission. The most conspicuous examples are found in ants of the Camponotini tribe, colloquially known as 'zombie ants'. While the behaviours induced during infection are well described, their molecular underpinnings remain unknown. Recent genomics and transcriptomics analyses of Ophiocordyceps camponoti-floridani have identified several highly upregulated biomolecules produced by the fungus during infection of Camponotus floridanus. Among them is an ergot alkaloid related to the mycotoxin aflatrem, known to cause 'staggers syndrome' in cows. Staggering, defined as unsteady movements side to side, is also observed in C. floridanus ants during late-stage infection. To test whether aflatrem-like compounds could be responsible, we injected healthy ants with aflatrem and recorded their behaviour for 30 min. Using both the automated object-tracking software MARGO and manual behavioural quantification, we found that aflatrem reduced ant activity and speed and increased staggering behaviours. To examine underlying transcriptomic changes, we performed RNA-seq on the heads of aflatrem-injected ants, keeping in step with previous transcriptomic work on Ophiocordycepsmanipulated ants. We identified 261 genes that were significantly dysregulated in the aflatrem-injected ants compared to sham-injected controls. When compared with RNA-seq data from Ophiocordycepsmanipulated ants, we found that both groups shared 113 differentially regulated genes. These included sensory neuron membrane protein genes, several odorant-binding protein genes and musculoskeletal genes such as titin and obscurin. Together, these results indicate that aflatrem-like compounds significantly affect neuromuscular and sensory function in C. floridanus. The conservation of staggers phenotype between C. floridanus and Bos taurus suggests that behaviour-manipulating strategies exhibited across the Tree of Life may be more similar in approach, if not widely different in application, than we realize.(c) 2023 The Author(s). Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour. This is an open access article under the CC BY license (http://creativecommons.org/licenses/ by/4.0/).