Social transfer of pathogenic fungus promotes active immunisation in ant colonies.
Social transfer of pathogenic fungus promotes active immunisation in ant colonies.
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DOI：
10.1371/journal.pbio.1001300
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发表时间：
2012
期刊：
影响因子：
9.8
通讯作者：
Cremer S
中科院分区：
文献类型：
--
作者：
Konrad M;Vyleta ML;Theis FJ;Stock M;Tragust S;Klatt M;Drescher V;Marr C;Ugelvig LV;Cremer S
与暴露在真菌中的蚂蚁进行社会接触会导致病原体转移到健康的蚁穴中，导致低水平的感染。这些微感染促进了病原体特异性免疫基因的表达，并促进了巢友的保护性免疫。由于流行病的无处不在的风险，昆虫协会在个体和群体层面上进化出了复杂的疾病防御系统。一个有趣但鲜为人知的现象是，与接触病原体的个体的社会接触降低了以前幼稚的筑巢伙伴对这种病原体的易感性。我们测试了Lasius蚂蚁对昆虫病原真菌金龟子绿僵菌的这种社会免疫是基于与受感染的个体接触后巢友免疫系统的主动上调，还是基于通过在群体成员之间转移免疫效应器的被动保护-即主动免疫和被动免疫。我们没有发现通过在群体成员之间转移抗菌剂而参与被动免疫的证据。相反，在幼稚蚂蚁和暴露于病原体的蚂蚁之间，在真菌分生孢子牢牢附着在它们的角质层之前，它们之间密集的同种异体梳理行为表明，病原体从暴露的个体传给了它们的筑巢伙伴。通过追踪荧光标记的分生孢子，我们确实检测到病原体频繁地转移到巢中，在那里它们引起低水平的感染，从它们解剖的身体内容物中生长出少量的真菌菌落形成单位。这些感染很少导致死亡，相反，它们促进了抑制真菌生长的能力增强，以及参与抗真菌防御的免疫基因(防御素和酚氧化酶原，PPO)的活跃上调。相反，与抗菌和抗病毒防御相关的组织蛋白L基因没有上调，我们也没有发现暴露在真菌中的蚂蚁的巢内抗菌活性增加。这表明真菌暴露后的社会免疫是特定的，类似于最近在无脊椎动物中进行个人水平免疫启动的发现。流行病学模型进一步表明，主动社会免疫具有适应性，因为它比被动免疫导致更快地消除疾病和更低的死亡率。有趣的是，人类还利用低水平感染的保护作用，通过有意转移低病原体剂量(“接种”或“接种”)来抗击天花。密切的社会接触促进了病原体在社会中的传播，往往会导致流行病。与此相反，我们证明了真菌病原体在蚂蚁群体中的有限传播对宿主是有益的，因为它促进了健康群体成员的“社会免疫”。我们发现，暴露在这种真菌下的蚂蚁会被它们健康的巢友大量梳理。美容可以从暴露的蚂蚁体内去除大量的真菌分生孢子，降低它们生病的风险。与此同时，以前健康的巢友自己也暴露在少量的分生孢子中，引发了低水平的感染。这些微感染不是致命的，但会导致一组特定免疫基因的上调表达和病原体特异性保护性免疫刺激。因此，通过社会相互作用进行病原体转移是蚂蚁社会对真菌感染进行社会免疫的基本机制。这种自然的社会免疫与人类诱导对致命疾病(如天花)免疫的努力有相似之处。在发明死亡或减毒株疫苗之前，人类社会的免疫是通过主动传播低水平感染(“变异”)来诱导的，就像蚂蚁一样。
Social contact with fungus-exposed ants leads to pathogen transfer to healthy nest-mates, causing low-level infections. These micro-infections promote pathogen-specific immune gene expression and protective immunization of nest-mates. Due to the omnipresent risk of epidemics, insect societies have evolved sophisticated disease defences at the individual and colony level. An intriguing yet little understood phenomenon is that social contact to pathogen-exposed individuals reduces susceptibility of previously naive nestmates to this pathogen. We tested whether such social immunisation in Lasius ants against the entomopathogenic fungus Metarhizium anisopliae is based on active upregulation of the immune system of nestmates following contact to an infectious individual or passive protection via transfer of immune effectors among group members—that is, active versus passive immunisation. We found no evidence for involvement of passive immunisation via transfer of antimicrobials among colony members. Instead, intensive allogrooming behaviour between naive and pathogen-exposed ants before fungal conidia firmly attached to their cuticle suggested passage of the pathogen from the exposed individuals to their nestmates. By tracing fluorescence-labelled conidia we indeed detected frequent pathogen transfer to the nestmates, where they caused low-level infections as revealed by growth of small numbers of fungal colony forming units from their dissected body content. These infections rarely led to death, but instead promoted an enhanced ability to inhibit fungal growth and an active upregulation of immune genes involved in antifungal defences (defensin and prophenoloxidase, PPO). Contrarily, there was no upregulation of the gene cathepsin L, which is associated with antibacterial and antiviral defences, and we found no increased antibacterial activity of nestmates of fungus-exposed ants. This indicates that social immunisation after fungal exposure is specific, similar to recent findings for individual-level immune priming in invertebrates. Epidemiological modeling further suggests that active social immunisation is adaptive, as it leads to faster elimination of the disease and lower death rates than passive immunisation. Interestingly, humans have also utilised the protective effect of low-level infections to fight smallpox by intentional transfer of low pathogen doses (“variolation” or “inoculation”). Close social contact facilitates pathogen transmission in societies, often causing epidemics. In contrast to this, we show that limited transmission of a fungal pathogen in ant colonies can be beneficial for the host, because it promotes “social immunisation” of healthy group members. We found that ants exposed to the fungus are heavily groomed by their healthy nestmates. Grooming removes a significant number of fungal conidiospores from the body surface of exposed ants and reduces their risk of falling sick. At the same time, previously healthy nestmates are themselves exposed to a small number of conidiospores, triggering low-level infections. These micro-infections are not deadly, but result in upregulated expression of a specific set of immune genes and pathogen-specific protective immune stimulation. Pathogen transfer by social interactions is therefore the underlying mechanism of social immunisation against fungal infections in ant societies. There is a similarity between such natural social immunisation and human efforts to induce immunity against deadly diseases, such as smallpox. Before vaccination with dead or attenuated strains was invented, immunity in human societies was induced by actively transferring low-level infections (“variolation”), just like in ants.
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影响因子：
1.3
作者：
Baer, B;Krug, A;Hughes, WOH
通讯作者：
Hughes, WOH
影响因子：
3.7
作者：
Cremer, Sylvia;Ugelvig, Line V.;Drijfhout, Falko P.;Schlick-Steiner, Birgit C.;Steiner, Florian M.;Seifert, Bernhard;Hughes, David P.;Schulz, Andreas;Petersen, Klaus S.;Konrad, Heino;Stauffer, Christian;Kiran, Kadri;Espadaler, Xavier;d'Ettorre, Patrizia;Aktac, Nihat;Eilenberg, Jorgen;Jones, Graeme R.;Nash, David R.;Pedersen, Jes S.;Boomsma, Jacobus J.
通讯作者：
Boomsma, Jacobus J.
影响因子：
2.2
作者：
Armitage, Sophie A. O.;Boomsma, Jacobus J.
通讯作者：
Boomsma, Jacobus J.
影响因子：
15.1
作者：
Aubert, A.;Richard, F. -J.
通讯作者：
Richard, F. -J.
影响因子：
4
作者：
Hauton, Chris;Smith, Valerie J.
通讯作者：
Smith, Valerie J.