Tsetse immune system maturation requires the presence of obligate symbionts in larvae.

Tsetse immune system maturation requires the presence of obligate symbionts in larvae.
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DOI:
10.1371/journal.pbio.1000619
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发表时间:
2011-05
期刊:
影响因子:
9.8
通讯作者:
Aksoy S
Aksoy S
中科院分区:
生物学1区
文献类型:
--
作者:
Weiss BL;Wang J;Aksoy S

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采采蝇体内有一种专性共生体,即Wigglesophagia glossinidia,它必须存在于幼虫成熟期间,以使果蝇的免疫系统在成年期正常发育和发挥功能。有益的微生物共生体在其宿主中发挥重要作用,包括膳食补充和维持免疫系统稳态。关于使这些细菌能够在发育期间和成年期诱导特定宿主表型的机制知之甚少。在这里,我们使用采采蝇,Glossina morsitans,和它的专性互利,Wigglesophagia glossinidia,调查的共同进化的适应,影响主机的生理过程的发展。摇摆病是通过乳汁腺分泌物由母体传染给采采蝇宫内幼虫的。我们可以培育出缺乏Wigglesophagia(GmmWgm −)的果蝇,但保留了其他共生微生物。这样的后代产生的成年人表现出很大程度上正常的表型,除了他们是生殖不育。我们的研究结果表明,当在正常环境条件下饲养时,GmmWgm −成虫也是免疫功能低下的,对血腔E高度敏感。大肠杆菌感染,而年龄匹配的野生型个体是难治的。在幼虫发育过程中缺乏Wigglesophagia的成虫在微生物挑战后表现出异常受损的细胞和体液免疫应答,包括编码抗菌肽(天蚕素和attacin)的基因表达减少,血细胞介导的过程(含硫酯蛋白2和4以及酚氧化酶原)和信号介导分子(诱导型一氧化氮合酶)。此外,GmmWgm −成虫的固着和循环血细胞数量减少,这一现象可能是由于幼虫的蛇形和菱形表达显著减少所致,这两者都与早期血细胞分化过程有关。我们的研究结果表明,Wigglesophoria必须存在于未成熟后代的发展过程中,以使免疫系统在成年舌蝇中正常发挥作用。这一现象提供了另一个重要的生理适应的证据,进一步锚定采采蝇和Wiggleschiaria之间的专性共生。有益的细菌共生体在自然界中普遍存在,其特征通常在于它们与宿主相互作用的程度。在互惠共生的情况下,双方都受益,这样每个人都可以居住在不同的生态位,没有一个可以单独生存。不幸的是,我们对互惠关系背后的功能机制知之甚少。昆虫代表了一组先进的多细胞生物体,具有良好的记录共生协会。采采蝇就是这样一种昆虫,它体内有一种母体传播的细菌互利共生体,称为Wiggleschiaria,为宿主提供脊椎动物血液特异性饮食中所缺少的必需代谢物。在这项研究中,我们通过研究这种细菌与宿主免疫系统之间的相互作用,进一步研究了采采蝇和Wigglesophagia之间的关系。我们已经发现,当Wigglesophoria是缺席采采蝇在成熟的未成熟的幼虫阶段,随后的成年人的特点是不发达的细胞免疫系统,因此非常容易感染一个正常的非致病性的外来微生物。这些发现代表了一种额外的适应,进一步巩固了采采蝇与其专性共生体之间的稳固关系。
Tsetse harbors an obligate symbiont, Wigglesworthia glossinidia, that must be present during larval maturation for the fly's immune system to develop and function properly during adulthood. Beneficial microbial symbionts serve important functions within their hosts, including dietary supplementation and maintenance of immune system homeostasis. Little is known about the mechanisms that enable these bacteria to induce specific host phenotypes during development and into adulthood. Here we used the tsetse fly, Glossina morsitans, and its obligate mutualist, Wigglesworthia glossinidia, to investigate the co-evolutionary adaptations that influence the development of host physiological processes. Wigglesworthia is maternally transmitted to tsetse's intrauterine larvae through milk gland secretions. We can produce flies that lack Wigglesworthia (GmmWgm −) yet retain their other symbiotic microbes. Such offspring give rise to adults that exhibit a largely normal phenotype, with the exception being that they are reproductively sterile. Our results indicate that when reared under normal environmental conditions GmmWgm − adults are also immuno-compromised and highly susceptible to hemocoelic E. coli infections while age-matched wild-type individuals are refractory. Adults that lack Wigglesworthia during larval development exhibit exceptionally compromised cellular and humoral immune responses following microbial challenge, including reduced expression of genes that encode antimicrobial peptides (cecropin and attacin), hemocyte-mediated processes (thioester-containing proteins 2 and 4 and prophenoloxidase), and signal-mediating molecules (inducible nitric oxide synthase). Furthermore, GmmWgm − adults harbor a reduced population of sessile and circulating hemocytes, a phenomenon that likely results from a significant decrease in larval expression of serpent and lozenge, both of which are associated with the process of early hemocyte differentiation. Our results demonstrate that Wigglesworthia must be present during the development of immature progeny in order for the immune system to function properly in adult tsetse. This phenomenon provides evidence of yet another important physiological adaptation that further anchors the obligate symbiosis between tsetse and Wigglesworthia. Beneficial bacterial symbionts, which are ubiquitous in nature, are often characterized by the extent to which they interact with the host. In the case of mutualistic symbioses, both partners benefit so that each one can inhabit diverse ecological niches where neither could survive on its own. Unfortunately, little is known about the functional mechanisms that underlie mutualistic relationships. Insects represent a group of advanced multi-cellular organisms that harbor well-documented symbiotic associations. One such insect, the tsetse fly, harbors a maternally transmitted bacterial mutualist called Wigglesworthia that provides its host with essential metabolites missing from its vertebrate blood-specific diet. In this study, we further examine the relationship between tsetse and Wigglesworthia by investigating the interaction between this bacterium and its host's immune system. We have found that when Wigglesworthia is absent from tsetse during the maturation of immature larval stages, subsequent adults are characterized by an underdeveloped cellular immune system and thus highly susceptible to infection with a normally non-pathogenic foreign microbe. These findings represent an additional adaptation that further anchors the steadfast relationship shared between tsetse and its obligate symbiont.
DOI: 10.1007/pl00006444
发表时间: 1999-01-01
影响因子: 3.9
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